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Convergent gene loss in aquatic plants predicts new components of plant immunity and drought response

EL Baggs, AS Thanki, R O’Grady, C Schudoma, W Haerty, KV Krasileva
doi: https://doi.org/10.1101/572560
EL Baggs
1Earlham Institute, Norwich Research Park, Norwich, NR4 7UZ, United Kingdom
2University of California Berkeley, Berkeley, California, 94720, United States of America
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AS Thanki
1Earlham Institute, Norwich Research Park, Norwich, NR4 7UZ, United Kingdom
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R O’Grady
3The Sainsbury Laboratory, Norwich Research Park, Norwich, NR4 7UH, United Kingdom
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C Schudoma
1Earlham Institute, Norwich Research Park, Norwich, NR4 7UZ, United Kingdom
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W Haerty
1Earlham Institute, Norwich Research Park, Norwich, NR4 7UZ, United Kingdom
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KV Krasileva
1Earlham Institute, Norwich Research Park, Norwich, NR4 7UZ, United Kingdom
2University of California Berkeley, Berkeley, California, 94720, United States of America
3The Sainsbury Laboratory, Norwich Research Park, Norwich, NR4 7UH, United Kingdom
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  • For correspondence: kseniak@berkeley.edu
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Abstract

The transition of plants from sea to land sparked an arms race with pathogens. The increased susceptibility of land plants is largely thought to be due to their dependence on micro-organisms for nutrients; the ensuing co-evolution has shaped the plant immune system. By profiling the immune receptors across flowering plants, we identified species with low numbers of NLR immune receptors. Interestingly, four of these species represent distinct lineages of monocots and dicots that returned to the aquatic lifestyle. Both aquatic monocot and dicot species lost the same well-known downstream immune signalling complex (EDS1-PAD4). This observation inspired us to look for other genes with a similar loss pattern and allowed us to predict putative new components of plant immunity. Gene expression analyses confirmed that a group of these genes was differentially expressed under pathogen infection. Excitingly, another subset of these genes was differentially expressed upon drought. Collectively, our study reveals the minimal plant immune system required for life under water, and highlights additional components required for the life of land plants.

Author summary Plant resistance to pathogens is commonly mediated by a complex gene family, known as NLRs. Upon pathogen infection, changes in the cellular environment trigger NLR activation and subsequent defence responses. Despite the dependence of agricultural practices on NLR genes to control pathogen load, relatively little is known about this gene family outside of model crop species. In this study, we identified a convergent reduction in the NLR gene family among two lineages of aquatic plants. Furthermore, we established that NLR reduction occurred in conjunction with the loss of a common immune signalling pathway. Subsequently, we identified other genes convergently lost in aquatic species and propose these as candidate components of the plant immune signalling pathway. In addition, we revealed components of the agronomically important drought response to be lost in aquatic plants. This study adds to our understanding of the complex interactions between environment and response to biotic stress, widely known as the disease triangle. The pathways identified in this study shed further light on the link between responses to drought and disease.

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted March 11, 2019.
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Convergent gene loss in aquatic plants predicts new components of plant immunity and drought response
EL Baggs, AS Thanki, R O’Grady, C Schudoma, W Haerty, KV Krasileva
bioRxiv 572560; doi: https://doi.org/10.1101/572560
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Convergent gene loss in aquatic plants predicts new components of plant immunity and drought response
EL Baggs, AS Thanki, R O’Grady, C Schudoma, W Haerty, KV Krasileva
bioRxiv 572560; doi: https://doi.org/10.1101/572560

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